Biomaterial evolution parallels behavioral innovation in the origin of orb-like spider webs

Correlated evolution of traits can act synergistically to facilitate organism function. But, what happens when constraints exist on the evolvability of some traits, but not others? The orb web was a key innovation in the origin of >12,000 species of spiders. Orb evolution hinged upon the origin of novel spinning behaviors and innovations in silk material properties. In particular, a new major ampullate spidroin protein (MaSp2) increased silk extensibility and toughness, playing a critical role in how orb webs stop flying insects. Here, we show convergence between pseudo-orb-weaving Fecenia and true orb spiders. As in the origin of true orbs, Fecenia dragline silk improved significantly compared to relatives. But, Fecenia silk lacks the high compliance and extensibility found in true orb spiders, likely due in part to the absence of MaSp2. Our results suggest how constraints limit convergent evolution and provide insight into the evolution of nature's toughest fibers.

[1]  M. Kuntner,et al.  Ladder webs in orb-web spiders: ontogenetic and evolutionary patterns in Nephilidae , 2010 .

[2]  Ryan Reza,et al.  Spider minor ampullate silk proteins are constituents of prey wrapping silk in the cob weaver Latrodectus hesperus. , 2008, Biochemistry.

[3]  H. W. Levi.  The spider genera Psechrus and Fecenia (Araneae : Psechridae) , 1982 .

[4]  N. Ayoub,et al.  Untangling spider silk evolution with spidroin terminal domains , 2010, BMC Evolutionary Biology.

[5]  Steffen Bayer.  Revision of the pseudo-orbweavers of the genus Fecenia Simon, 1887 (Araneae, Psechridae), with emphasis on their pre-epigyne , 2011, ZooKeys.

[6]  Ingi Agnarsson,et al.  The Form and Function of Spider Orb Webs: Evolution from Silk to Ecosystems , 2011 .

[7]  S. O. Andersen.  Amino acid composition of spider silks , 1970 .

[8]  R. Lewis,et al.  Evidence from flagelliform silk cDNA for the structural basis of elasticity and modular nature of spider silks. , 1998, Journal of molecular biology.

[9]  J. Gosline,et al.  The mechanical design of spider silks: from fibroin sequence to mechanical function. , 1999, The Journal of experimental biology.

[10]  R. Lewis,et al.  Structure of a protein superfiber: spider dragline silk. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[11]  G. Plaza,et al.  Supercontraction of dragline silk spun by lynx spiders (Oxyopidae). , 2010, International journal of biological macromolecules.

[12]  Manuel Elices,et al.  Mechanical behavior of silk during the evolution of orb-web spinning spiders. , 2009, Biomacromolecules.

[13]  O. Gascuel,et al.  A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. , 2003, Systematic biology.

[14]  Y. Termonia.  Molecular modeling of spider silk elasticity , 1994 .

[15]  Y. Lubin,et al.  SPECIALISTS AND GENERALISTS: THE ECOLOGY AND BEHAVIOR OF SOME WEB-BUILDING SPIDERS FROM PAPUA NEW GUINEA IL Psechrus argentatus and Fecenia sp. (Araneae: Psechridae) , 2006 .

[16]  R. Lewis,et al.  Molecular architecture and evolution of a modular spider silk protein gene. , 2000, Science.

[17]  Markus J. Buehler,et al.  Nonlinear material behaviour of spider silk yields robust webs , 2012, Nature.

[18]  T. Blackledge.  Prey capture in orb weaving spiders: are we using the best metric? , 2011 .

[19]  G. Turner.  The Ecology of Adaptive Radiation , 2001, Heredity.

[20]  J. Coddington,et al.  Phylogeny of the orb-web building spiders (Araneae, Orbiculariae: Deinopoidea, Araneoidea) , 1998 .

[21]  Todd A. Blackledge,et al.  Variation in the material properties of spider dragline silk across species , 2006 .

[22]  Adam P. Summers,et al.  SPIDER DRAGLINE SILK: CORRELATED AND MOSAIC EVOLUTION IN HIGH-PERFORMANCE BIOLOGICAL MATERIALS , 2006, Evolution; international journal of organic evolution.

[23]  W. Shear,et al.  Spiders : webs, behavior, and evolution , 1986 .

[24]  D. Dimitrov,et al.  Tangled in a sparse spider web: single origin of orb weavers and their spinning work unravelled by denser taxonomic sampling , 2012, Proceedings of the Royal Society B: Biological Sciences.

[25]  N. Pierce,et al.  Evidence for diet effects on the composition of silk proteins produced by spiders. , 2000, Molecular biology and evolution.

[26]  Andrew T. Sensenig,et al.  Behavioural and biomaterial coevolution in spider orb webs , 2010, Journal of evolutionary biology.

[27]  John P. Huelsenbeck,et al.  MRBAYES: Bayesian inference of phylogenetic trees , 2001, Bioinform..

[28]  Samuel Venner,et al.  Spider webs designed for rare but life-saving catches , 2005, Proceedings of the Royal Society B: Biological Sciences.

[29]  Hsuan-Chen Wu,et al.  Giant wood spider Nephila pilipes alters silk protein in response to prey variation , 2005, Journal of Experimental Biology.

[30]  M. Kuntner,et al.  The phylogenetic placement of Psechridae within Entelegynae and the convergent origin of orb‐like spider webs , 2013 .

[31]  A. Bennett.  The Origin of Species by means of Natural Selection; or the Preservation of Favoured Races in the Struggle for Life , 1872, Nature.

[32]  D. Maddison,et al.  Mesquite: a modular system for evolutionary analysis. Version 2.6 , 2009 .

[33]  D. Kaplan,et al.  The amino acid composition of major ampullate gland silk (dragline) of Nephila clavipes (Araneae, Tetragnathidae). , 1990 .

[34]  S. Zschokke,et al.  Asymmetry in Orb-Webs: An Adaptation to Web Building Costs? , 2008, Journal of Insect Behavior.

[35]  Rob DeSalle,et al.  Combined support for wholesale taxic atavism in gavialine crocodylians. , 2003, Systematic biology.

[36]  D. Porter,et al.  Proline and processing of spider silks. , 2008, Biomacromolecules.

[37]  Andrew M. Smith,et al.  Decoding the secrets of spider silk , 2011 .

[38]  D. Kaplan,et al.  Purification and characterization of recombinant spider silk expressed in Escherichia coli , 1998, Applied Microbiology and Biotechnology.

[39]  Sean P Kelly,et al.  Spider orb webs rely on radial threads to absorb prey kinetic energy , 2012, Journal of The Royal Society Interface.

[40]  N. Platnick,et al.  Towards a Phylogeny of Entelegyne Spiders (Araneae, Araneomorphae, Entelegynae) , 1999 .

[41]  M. Herberstein,et al.  Asymmetry in spider orb webs: a result of physical constraints? , 1999, Animal Behaviour.

[42]  M B Hinman,et al.  Isolation of a clone encoding a second dragline silk fibroin. Nephila clavipes dragline silk is a two-protein fiber. , 1992, The Journal of biological chemistry.

[43]  C. Hayashi,et al.  Early Events in the Evolution of Spider Silk Genes , 2012, PloS one.

[44]  Sarah Rauscher,et al.  Proline and glycine control protein self-organization into elastomeric or amyloid fibrils. , 2006, Structure.

[45]  D. Schluter,et al.  Ecological Character Displacement and Speciation in Sticklebacks , 1992, The American Naturalist.

[46]  E. Bongcam-Rudloff,et al.  Major ampullate spidroins from Euprosthenops australis: multiplicity at protein, mRNA and gene levels , 2007, Insect molecular biology.

[47]  R. Lewis,et al.  Hypotheses that correlate the sequence, structure, and mechanical properties of spider silk proteins. , 1999, International journal of biological macromolecules.

[48]  Sean P Kelly,et al.  Damping capacity is evolutionarily conserved in the radial silk of orb-weaving spiders. , 2011, Zoology.

[49]  R. Lewis,et al.  Extreme Diversity, Conservation, and Convergence of Spider Silk Fibroin Sequences , 2001, Science.

[50]  C. Craig.  Spiderwebs and silk : tracing evolution from molecules to genes to phenotypes , 2003 .

[51]  Ingi Agnarsson,et al.  Bioprospecting Finds the Toughest Biological Material: Extraordinary Silk from a Giant Riverine Orb Spider , 2010, PloS one.

[52]  Z. Shao,et al.  Elasticity of spider silks. , 2008, Biomacromolecules.

[53]  David L Kaplan,et al.  Silk-based biomaterials. , 2003, Biomaterials.

[54]  Jonathan A Coddington,et al.  Reconstructing web evolution and spider diversification in the molecular era , 2009, Proceedings of the National Academy of Sciences.

[55]  Manuel Elices,et al.  Sequential origin in the high performance properties of orb spider dragline silk , 2012, Scientific Reports.

[56]  D. Posada.  jModelTest: phylogenetic model averaging. , 2008, Molecular biology and evolution.

[57]  J. Bond,et al.  TESTING ADAPTIVE RADIATION AND KEY INNOVATION HYPOTHESES IN SPIDERS , 1998, Evolution; international journal of organic evolution.